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Home , Caenolestes, Deseadan, Itaboraian, Mimoperadectes, Paucituberculata, Shrew opossum

Swiss J Palaeontol DOI 10.1007/s13358-014-0063-9

An exceptionally well-preserved skeleton of Palaeothentes from the Early of , : new insights into the anatomy of extinct paucituberculatan

Analia M. Forasiepi • Marcelo R. Sa´nchez-Villagra • Thomas Schmelzle • Sandrine Ladeve`ze • Richard F. Kay

Received: 8 September 2013 / Accepted: 13 February 2014 Ó Akademie der Naturwissenschaften Schweiz (SCNAT) 2014

Abstract During the Cenozoic paucituberculatans were an anterior semicircular canal (SC) projecting slightly much more diverse taxonomically and ecomorphologically dorsally from the dorsal-most point of the posterior SC, and than the three extant genera of -like marsupials. lateral and posterior SCs projecting laterally to the same Among paucituberculatans, palaeothentids were abundant level. On the basis of postcranial anatomy, previous studies during the Early Miocene, although most of the fossil have demonstrated that P. lemoinei was an agile cursorial remains consist of isolated teeth or fragmentary jaws. We form, an inference supported by study of the new post- describe a new and exceptional partial skeleton of Palaeo- cranial elements. thentes lemoinei (Palaeothentidae), collected from the Santa Cruz Formation ( age, Early Miocene) Keywords Marsupialia Á Á Cenozoic Á in Patagonia. Whereas the skull of P. lemoinei has more South America Á Skull Á Inner ear Á Postcranium plesiomorphic traits in the face, palate, and cranial vault than that of living paucituberculatans, the dental mor- Abbreviations phology is more derived. The osseous inner ear was examined using micro-CT scanning, revealing a cochlea Institutional abbreviations with 1.9 turns, the presence of a ‘‘second crus commune’’, FMNH Field Museum of Natural History, Chicago, USA IEEUACH Universidad Austral de , A. M. Forasiepi Instituto de Ecologı´a y Evolucio´n, Instituto Argentino de Nivologı´a, Glaciologı´a y Ciencias Valdivia, Chile Ambientales, CCT-Mendoza, CONICET, Av. Ruiz Leal s/no, MACN-A Museo Argentino de Ciencias 5500 Mendoza, Argentina Naturales ‘‘Bernardino Rivadavia’’, A. M. Forasiepi Á M. R. Sa´nchez-Villagra (&) Ameghino Collection, Buenos Aires, Palaeontological Institute and Museum, University of Zu¨rich, Argentina Karl Schmid-Strasse 4, 8006 Zu¨rich, Switzerland MNHN-Pal-Bol-V Museo Nacional de Historia Natural, e-mail: [email protected] , La Paz, T. Schmelzle MPM-PV Museo Regional Provincial ‘‘Padre Fleckensteinstraße 7, 74206 Bad Wimpfen, Germany M. Jesu´s Molina’’, Rı´o Gallegos, Argentina S. Ladeve`ze PU Princeton University collections at Muse´um national d’Histoire naturelle, UMR 7207 CR2P CNRS/ MNHN/UPMC, 8, rue Buffon, CP38, 75231 Paris Cedex 05, Yale University, USA France Anatomical abbreviations R. F. Kay (&) I/i Upper and lower incisor Department of Evolutionary Anthropology, Duke University, C/c Upper and lower canine Durham, NC 27708-03083, USA P/p Upper and lower premolar e-mail: [email protected] A. M. Forasiepi et al.

M/m Upper and lower molar Villagra 2003; Asher et al. 2004; Nilsson et al. 2004, 2010; ASC Anterior semicircular canal Beck et al. 2008; Horovitz et al. 2008, 2009; Meredith et al. LSC Lateral semicircular canal 2008). Other studies located paucituberculatans at the base PSC Posterior semicircular canal of Marsupialia (e.g., Szalay 1994; Baker et al. 2004; Meredith et al. 2009, 2011) or provided the two alternatives (Beck 2008). Consequently, the understanding of the Introduction anatomy of fossil paucituberculatans has the potential to provide new data to interpret the anatomy and the character is a clade of shrew-like marsupials evolution of the Australian marsupials or early marsupials. endemic to South America. The group includes seven Unfortunately, the fossil record of paucituberculatans is extant small and insectivorous arranged in three mainly confined to teeth. genera: , Lestoros, and Rhyncholestes (Wilson Paucituberculatans are typically classified into the Lin- and Reeder 1993; Ojala-Barbour et al. 2013). Fossil naean families Caenolestidae, which includes the living members of this group were much more diverse taxo- taxa, and the extinct Pichipilidae, Abderitidae and Palaeo- nomically and ecomorphologically (Marshall 1980; Bown thentidae, and stem taxa (Marshall 1980; Bown and Fleagle and Fleagle 1993; Abello 2007; Abello and Candela 2010) 1993; Abello 2007, 2013; Goin et al. 2009; Abello 2013; and are known since the Early Eocene ( age) Fig. 1). Palaeothentidae occurred from the late (Goin et al. 2009; Abello 2013; Fig. 1). to the middle Miocene ( to ages) in The alpha and the phylogenetic relationships , Bolivia, southern Argentina, and Chile (Mar- of paucituberculatans has been thoroughly revised (Abello shall 1980; Bown and Fleagle 1993; Dumont and Bown 2007, 2013) and continues to be studied (Goin et al. 2010; 1997; Abello 2007, 2013). Palaeothentids were abundant Abello and Rubilar-Rogers 2012). The discovery of early during the late Early Miocene (Santacrucian age), with paucituberculatans and closer relatives (Goin et al. 2007, Palaeothentes being the most speciose , with five 2009; Forasiepi et al. 2013) significantly increases the species: P. aratae, P. intermedius, P. lemoinei, P. minutus, understanding of the character evolution within this clade. and P. pascuali. Despite an extensive fossil record, com- Several studies based on molecular, morphological, and plete skulls and skeletons are rare. Most of the fossil combined data agree that paucituberculatans are the sister remains consist of isolated teeth, fragmentary mandibles taxa of (e.g., Horovitz and Sa´nchez- and fragmentary maxillae (Abello 2007). To date, four

Fig. 1 Phylogenetic relationships of several paucituberculatans based younger): Itab Itaboraian, Cas , SRF Santa Rosa Fauna, on Abello (2013), indicating Palaeothentinae (the monophyletic group Tin ; Des Deseadan, Col , P Pinturan to Palaeothentes lemoinei belongs) in bold upper case. South fauna; S–F–C Santacrucian, , and , Lav Laventan, American Land Ages (S) are as follows (from older to Huay , Mon Montermosan Skeleton of the Palaeothentes lemoinei skulls of palaeothentids have been described. One belongs easier comparison. For the description, the lateral semi- to the Santacrucian palaeothentid Palaeothentes minutus circular canal was oriented horizontally and at the centre of (MACN-A 8271), and was damaged subsequent to its the anatomical structures (Graf and Klam 2006). The turns illustration by Ameghino (1887, p. 6; see also Marshall of the cochlea were counted following the protocol of West 1980, fig 20). Two other partial skulls assignable to the (1985). acdestid Acdestis oweni are also from the Santacrucian: specimens PU 15225 and FMNH 13160, the former described by Sinclair (1906)asPalaeothentes intermedius Systematic palaeontology and referred to Acdestis spegazzinii by Abello (2007). The fourth skull is from rocks of Laventan age of Bolivia Marsupialia Illiger 1811 (MNHN-Pal-Bol-V-4000) and was described as Acdestis Paucituberculata Ameghino 1894 maddeni (Goin et al. 2003). Palaeothentidae Sinclair 1906 This contribution describes and examines a new speci- Palaeothentes Ameghino 1887 men, comprising the skull and postcranial skeleton, of the P. lemoinei Ameghino 1887 palaeothentid P. lemoinei (MPM-PV 3566), collected from Holotype. MACN-A 3, fragment of right dentary with m1–m4. Puesto Estancia La Costa of the Estancia La Costa Mem- ber, Santa Cruz Formation (Santacrucian age). The speci- Occurrence and age. Santa Cruz, Pinturas, and Rı´o Frias men was recovered in 2003 by RFK during a joint formations, Early–Middle Miocene (Santacrucian–Friasian expedition from Museo de la Plata (Argentina) and Duke South American Land Mammal Ages), Patagonia, Argen- University (USA). This new specimen adds insights into tina and Chile (Marshall 1980, 1990; Bown and Fleagle the knowledge of the anatomy of extinct paucitubercula- 1993; Abello 2007). tans and is the core of the present study, focusing on the Referred specimen. MPM-PV 3566, skull with dentition, middle ear anatomy. We apply the techniques of CT complete left and fragment of right dentary with dentition, technology to study the internal osseous inner ear anatomy right petrosal, and postcranium (16 vertebrae, ribs, right pelvic of P. lemoinei and to undertake comparisons with other girdle, right femur, proximal fibula, right astragalus, left Metatheria. humerus, left ulna, both radii, metapodials, and phalanxes). Remarks. The combination of the following features per- Materials and methods mits allocation of MPM-PV 3566 to P. lemoinei (for a taxonomic revision of the genus and revised diagnosis see The nomenclature for the descriptions follows veterinary Abello 2007): wide crown bases in M1–M2, larger in molar text books (e.g., Schaller 1992) and particular publications size than the Santacrucian species P. intermedius, P. based on metatherians. The nomenclature for the skull pascuali, and P. minutus and smaller than in P. aratae follows Wible (2003), for the petrosal Wible (1990, 2003), (Abello 2007; Tables 18a–d), less steep molar-size gradi- for the inner ear Schmelzle et al. (2007), and for the den- ent from m1 to m4, and more protruding protocone on M1. tition Abello (2007, 2013). Additionally, P. lemoinei has the plesiomorphic traits of P1 The internal structure of the petrosal bone of P. lemoinei with two roots (unirradiculated in P. aratae) and a pro- was documented using a micro-CT-Scanner RayScan 200 portionally smaller m1 trigonid, and its corresponding P3 at the Fachhochschule Aalen, Germany. Caenolestes sp. counterpart (larger in P. aratae). was scanned at the Anthropological Institut and Museum of the University of Zu¨rich, (lCT80, Scanco Medical, Bas- sersdorf). The specimen of Dromiciops gliroides (IEEU- Description and comparisons ACH 2167) was scanned at the University of Poitiers (X8050-16 Viscom lCT scan). The resulting graphic files Skull were used to reconstruct the inner ear three-dimensionally using Avizo 8, VGStudio Max 1.1Ò and Materialise The skull is complete except for missing most of the right Mimics 16Ò (licence UMR7207). In order to generate a zygomatic arch, the anterior-most portion of the nasals, and virtual cast of the inner ear, a negative of the file was the posterior portion of the basicranium (Fig. 2). The skull produced and the software Cinema 4dÒ R8 XL (Losch preserves most of the upper dentition and portions of the et al. 1999) was used to delete the reconstructed areas of ear region, including an isolated right petrosal bone. the petrosal bone that cover the bony labyrinth. For Compared to extant paucituberculatans (Caenolestes: Caenolestes sp. and Dromiciops gliroides, the left petrosal mean for the different species range from 31 to 37 mm— was scanned but Figure 7 shows the mirrored inner ear for Ojala-Barbour et al. 2013—, Lestoros, mean about A. M. Forasiepi et al.

Fig. 2 Palaeothentid marsupial Palaeothentes lemoinei (MPM-PV 3566), from the late Early Miocene, Santa Cruz Formation, Patagonia, Argentina. Skull in dorsal (a), ventral (b), and lateral (c) views. Scale bar 10 mm

30 mm—Martin 2013—, and Rhyncholestes, mean about Table 1 Measurements of the skull and dentary (in mm) 33 mm—Osgood 1924; Patterson and Gallardo 1987), the Skull skull of P. lemoinei is much larger and with a shorter and Total (condylobasal) length 63a wider snout (Table 1). In lateral view, the premaxilla Maximum midline palatal length 39 makes a large contribution to the anterior part of the snout, Interorbital constriction width 7.8 as in other paucituberculatans, with a facial process that Maximum palate width (between lingual the side of M1) 12.3 represents more than 35 % of the total length of the snout Dentary (Fig. 2c). The most distal part of the premaxilla is broken, Maximum length 38.5a although the facets on the maxilla suggest that the facial Height at the level of the condylar process 10.2 process of the premaxilla is wedged between the maxilla Height at the level of the coronoid process 20.2 and nasal and projects posteriorly to the level of P2. As in other palaeothentids, there is no trace of an antorbital a The measurement is approximated Skeleton of the marsupial Palaeothentes lemoinei vacuity between the nasal and maxilla (Sinclair 1906; Goin parietals, from the level of the postorbital constriction to et al. 2003), a difference from caenolestids (Dederer 1909; the nuchal crest. The nuchal crests are tall and posteriorly Osgood 1921; Martin 2013). The remaining part of the projecting. The sagittal and nuchal crests are well defined snout is completed by the maxilla. A large infraorbital in fossil palaeothentids (Sinclair 1906; Goin et al. 2003). In foramen opens on the facial process and is located at the contrast, living caenolestids have no crests in this area of level of the posterior root of P3. The maxilla contacts the the skull. An interparietal is not an independent bone in P. frontal, in common with several stem marsupials (e.g., lemoinei, or any other adult caenolestids. It is likely fused , ; Marshall and Muizon 1995; to the parietals as this bone was found to be universal Horovitz et al. 2008) and most living marsupials. The among (Koyabu et al. 2012). The mid-frontal maxilla-jugal suture is nearly vertical. The zygomatic arch and mid-parietal sutures are partially observed, contrary to is deep dorsoventrally and robust, differing from the slen- adult and subadult Recent caenolestids in which these der arch found in caenolestids. The anterior root of the sutures are fused (Voss and Jansa 2009). zygoma is formed by the short zygomatic process of the The basisphenoid and alisphenoid are partially pre- maxilla. served (Fig. 2b). The carotid foramen opens latero-ven- In dorsal view (Fig. 2a), the nasals are narrow, although trally, just anterior to the suture with the basioccipital, in a less so than in living caenolestids (Osgood 1921; Martin manner similar to A. maddeni (Goin et al. 2003). The 2013). The nasals widen gradually posteriorly. The suture opening is large and oval. The transverse canal foramen is between nasals and frontals is W-shaped, with the frontal situated just anterior and lateral to the carotid foramen, as forming an anterior wedge. in most marsupials including caenolestids (Sa´nchez-Villa- In ventral view (Fig. 2b), the palate is narrow anteriorly gra and Wible 2002). The alisphenoid tympanic process is and wide at the level of M1–M2, with the molars arranged prominent and makes a contribution to the ossified auditory in arch. The anteriormost margin of the incisive foramen is bulla. Its contact with the rostral tympanic process of the missing (Fig. 3a), but it is evident that this foramen was petrosal, present in Caluromys and Caluromysiops (Voss large, similar to that of living caenolestids, with its pos- and Jansa 2009), is not possible to determine because the terior margin on the maxilla extending caudally to the petrosal was preserved detached from the skull. The fora- posterior border of P1 (Fig. 3b). The major palatine fora- men ovale is bordered anteriorly by the alisphenoid. men is contained in an extensive maxillopalatine vacuity, Because of incomplete preservation, it is not possible to although smaller than in living caenolestids (Osgood 1921; determine whether the foramen ovale was bordered by both Patterson and Gallardo 1987; Martin 2013). This vacuity the alisphenoid and the petrosal, as in most marsupials extends from the level of the M1–M3. Posteriorly and at including extant caenolestids, or if the foramen was the level of M4, there is another pair of small apertures, the entirely contained within the alisphenoid (e.g., Sa´nchez- posteromedial or palatine vacuity sensu Hershkovitz (1997) Villagra 2001; Voss and Jansa 2009). In posterior view, the opening close to the midline of the palate. The palate occipital area is flat, not globular as in living caenolestids. extends behind the M4. The posterior border of the palate Petrosal. The mammalian petrosal has two main divi- is straight and strengthened by the palatine torus (Fig. 2b). sions: the pars cochlearis, enclosing the auditory organ (the In lateral view (Fig. 2c), the facial process of the lacrimal cochlea), and the pars canalicularis, housing the organs of is small and restricted to the orbital rim. A single lacrimal the balance (the vestibular system) (Wible 2003). In tym- foramen was observed right by the orbital rim, as in living panic view (Figs. 4a, 5a), the pars cochlearis is represented caenolestids (Dederer 1909; Osgood 1921; Martin 2013). by the promontorium and anteromedial flange, while the The postorbital constriction, as observed in dorsal view pars canalicularis is represented by the bone posterior and (Fig. 2a), is deep, similar to the fossil palaeothentids Ac- lateral to the promontorium. The promotorium is bulbous destis maddeni (Goin et al. 2003) and Acdestis oweni and lacks grooves for vascular canals. The rostral tympanic (Sinclair 1906) and differing from living caenolestids, process is a short crest, concave laterally and taller poste- which have a very shallow constriction. The preorbital area riorly, as in Acdestis maddeni (Goin et al. 2003). However, is wide, as in other palaeothentids (Sinclair 1906; Goin the ridge of this crest-like process has a minimum of five et al. 2003), and comparable to the width of the braincase. small tubercles plus additional, smaller ones that are absent This differs from living caenolestids, which have broader in A. maddeni. The rostral tympanic process of P. lemoinei and more globular braincases. The temporal lines are low differs from the protruding finger-like process of didelphids and short, lacking contact with the sagittal crest (Fig. 2a). (Wible 2003) and even the low process of Caenolestes In P. minutus (Sinclair 1906), the temporal lines are (Sa´nchez-Villagra and Wible 2002). The anteromedial stronger than in P. lemoinei; in contrast, living caenolestids flange projects from the promontorium. This is a flat shelf lack these structures. In P. lemoinei, the sagittal crest in tympanic view, wider at its posterior base. The most extends on the midline of the skull, including frontals and anterior portion of this shelf is broken. The shallow A. M. Forasiepi et al.

Fig. 3 Palaeothentes lemoinei (MPM-PV 3566). Details of the premaxilla (a) and palate (b) with the upper dentition. Scale bar 5mm(a) and 10 mm (b)

Fig. 4 Palaeothentes lemoinei (MPM-PV 3566). Stereo pairs of the right petrosal in tympanic (a) and cerebellar (b) views. Scale bar 5mm elongated depression located lateral to the anteromedial hidden in tympanic view by the tall and robust caudal flange is recognised as the tensor tympani fossa for tympanic process (Figs. 4a, 5a). The fenestra vestibuli attachment of the tensor tympani muscle (Wible 2003). opens anterolateral to the fenestra cochleae. It is nearly Three main apertures are located posterior and lateral to circular in shape, with a length to width ratio (stapedial the promontorium: the fenestra cochleae posteromedially, ratio of Segall 1970) of 1.2, similar to that of other the fenestra vestibuli posterolaterally, and the secondary palaeothentids (Acdestis maddeni has a stapedial ratio of facial foramen laterally. The fenestra cochleae, for the 1.4; Goin et al. 2003). The shape of the fenestra vestibuli attachment of the secondary tympanic membrane, opens on conforms tightly to the shape of the footplate of the stapes the posterior wall of the promontorium and is partially (e.g., Archibald 1979). As such, the footplate of Skeleton of the marsupial Palaeothentes lemoinei

Fig. 5 Palaeothentes lemoinei (MPM-PV 3566). Model of the right (=oval window), hF hiatus Fallopii, iam internal acoustic meatus, mp petrosal based on 3D reconstructions from micro-CT data in tympanic mastoid process, n notch for the jugular foramen, pc prootic canal, (a) and cerebellar (b) views. ac aqueductus cochleae; amf, antero- ppts postpromontorial tympanic sinus, pr promontorium, ps sulcus for medial flange; asc, anterior semicircular canal; av aqueductus the prootic sinus, rtpp rostral tympanic process of petrosal, saf vestibuli, cc crus commune, cp crista parotica, crp crista petrosa, subarcuate fossa, sf stapedial fossa, sff secondary facial foramen, sips ctpp caudal tympanic process, er epitympanic recess, fai inferior sulcus for inferior petrosal sinus, sps sulcus for the superior petrosal acoustic foramen, fas superior acoustic foramen, fc fenestra cochleae sinus, th tympanohyal, ttf tensor tympani fossa (=round window), fi fossa incudis, fs facial sulcus, fv fenestra vestibuli

P. lemoinei would have been almost circular, as in most immediately posterior to the fenestra vestibuli. The stylo- living marsupials and stem therians (Archibald 1979; mastoid notch is well defined between the tympanohyal Wible 1990, 2003; Rougier et al. 1998; except Dromiciops, and the caudal tympanic process. There is a notch on the some other australidelphians, and didelphimorphians with a medial border of the postpromontorial tympanic sinus stapedial ratio larger than 1.8; Segall 1970; Horovitz and forming the lateral border of the jugular foramen (Figs. 4a, Sa´nchez-Villagra 2003; Horovitz et al. 2008). The crista 5a). As already mentioned, the caudal tympanic process is interfenestralis is wide and the fenestrae cochleae and the tall, resembling the condition of Caenolestes (Sa´nchez- fenestra vestibuli are widely separate. Villagra and Wible 2002). In tympanic view (Figs. 4a, 5a), the cavum supra- Lateral to the facial sulcus, there are two incompletely cochleare, which houses the geniculate ganglion, is cov- separated depressions: the epitympanic recess and the fossa ered by a bony bridge as in other metatherians (except incudis. The epitympanic recess, for the articulation of the juveniles and adult vombatids; Wible 1990; Rougier et al. malleus and incus, comprises a larger volume and is 1998). The hiatus Fallopii, for the exit of the greater located more anterior than the fossa incudis. The fossa petrosal nerve (a branch of the facial nerve), is small and incudis, for the short process of the incus, is deeper and located in the tympanic side of the petrosal, as in A. medially bordered by the crista parotica. The latter crest is maddeni (Goin et al. 2003) but differing from the dorsal short and increases its height medially. The crista parotica position of Caenolestes fuliginosus (Sa´nchez-Villagra and contacts the tympanohyal, a tall, robust process located Wible 2002). The secondary facial foramen, for the exit of posterior to the fenestra vestibuli. The tympanohyal (the the posterior branch of the facial nerve, is oval, slightly ossified Reichert’s cartilage) articulates with the stylohyal smaller than the fenestra vestibuli and opens posteroven- (the latter is not preserved in this specimen), joining the trally into the facial sulcus. The secondary facial foramen skull to the remaining elements of the hyoid apparatus and the fenestra vestibuli are adjacent. The facial sulcus is (Wible 2003). deep with parallel borders and oriented posteromedially A small canal lateral to the facial sulcus is interpreted towards the postpromontorial tympanic sinus. The post- here as the prootic canal (Figs. 4a, 5a). The prootic canal promontorial tympanic sinus is narrower and even deeper would connect the prootic sinus with the lateral head vein than the facial sulcus. The stapedial fossa, for the attach- (Wible 1990, 2003). The sulcus for the prootic sinus runs ment of the stapedius muscle, forms a small circular vertical on the mastoid process, in the squamosal view. The depression located in the postpromontorial tympanic sinus, mastoid process (i.e., the region posteromedial to the A. M. Forasiepi et al. caudal tympanic process of the petrosal) is irregular in impression of the inferior and superior petrosal venous shape and pierced by several small foramina. The mastoid sinuses. The impression for the inferior petrosal sinus is on process would have been partially exposed in occipital the anterior medial part of the petrosal, running antero- view as in the living caenolestids and most living marsu- posteriorly. The inferior petrosal sinus would drain the pials (Sa´nchez-Villagra and Wible 2002). Anterior to the blood into the internal jugular vein (e.g., Kay et al. 2008). promontorium and lateral to the anteromedial flange, the In agreement with the soft tissue that the depression would tympanic surface of the petrosal is pierced by several tiny convey, the sulcus for the inferior petrosal sinus in P. le- foramina (Figs. 4a, 5a). moinei extends to the level of the jugular notch. The sulcus In cerebellar view (Figs. 4b, 5b), two main depressions for the superior petrosal sinus is narrower and located are distinguished: the internal acoustic meatus and the anterior to the subarcuate fossa. subarcuate fossa. The internal acoustic meatus is deep and transversely wide. Inside the internal acoustic meatus, a Osseous inner ear. The osseous labyrinth consists of the broad crista transversa separates the superior acoustic cochlea, the vestibule, and the semicircular canals. The foramen anterolaterally from the inferior acoustic foramen cochlea comprises the largest part of the osseous labyrinth posteromedially (Figs. 4b, 5b). The crista transversa has a and contains the cochlear duct. minute vascular foramen leading into the petrosal. The In P. lemoinei, the cochlea coils with 1.9 turns, similar to superior acoustic foramen is oval and splits into two small Caenolestes sp. with 2 turns (Figs. 6d, 7d) The fenestra openings. The anterior aperture is the larger and corre- vestibuli is located ventral and slightly posterior to the sponds to the canal for the facial nerve; it is directed lateral ampulla (Fig. 6a, b). The cochlear canaliculus, ventrally, connecting the secondary facial foramen and which transmits the aqueductus cochleae, is short and nar- hiatus Fallopii. The anterior border of the superior acoustic row at its base. It opens at the posterior border of the foramen has a shallow notch that would represent the fenestra cochleae and extends medially. The fenestra passage of the facial nerve from the brain to the inner ear. cochleae is large and oval in shape. The vestibulum that The posterior aperture is partially hidden in cerebellar view contains the utricle and saccule is elongated (Fig. 6a, e). by the posterolateral border of the internal acoustic meatus The anterior, posterior, and lateral semicircular canals and would correspond to the aperture of the canal of the (ASC, PSC, and LSC) are almost complete except the ASC, vestibular nerve from the membranous labyrinth (e.g., which is partially broken. The ASC forms the rim of the Wible 2003). The inferior acoustic foramen is round and subarcuate fossa as seen in the cerebellar view of the has numerous small foramina of different size and random petrosal (Fig. 5b). The PSC is vertical and forms the medial distribution and corresponds to the cribriform tract for border of the subarcuate fossa; the LSC canal is in a per- passage of the fascicles of the cochlear nerve (Wible 1990, pendicular plane and forms its floor. The LSC is straight as 2003). The lateral border of the internal acoustic meatus seen in lateral view similar to Caenolestes (Fig. 6a, 7a), and delimits a blunt crest oriented posteromedially to the differing from the undulate shape of some diprotodontians anteromedial border of the subarcuate fossa. The crista (Phascolarctos and Vombatus; Schmelzle et al. 2007) and petrosa is even lower than the already mentioned crest Dromiciops (Fig. 7g). The angle between the ASC and PSC and is placed anterior to the internal acoustic meatus is 75° (measured on a plane parallel to the lateral semicir- (Figs. 4b, 5b). cular canal and with the crus commune in the hinge; The subarcuate fossa is deep, with well-defined borders, Fig. 6c). In Caenolestes, the angle is almost straight as in most metatherians (except large-sized taxa with (Fig. 7c). The angle between the PSC and LSC is 90° in P. shallow fossae; Sa´nchez-Villagra 2002) and would house lemoinei (measured on a plane parallel to the ASC; Fig. 6a), in life the cerebellar paraflocculus (e.g., MacIntyre 1972; similar to Caenolestes. The three semicircular canals of P. Wible 1990, 2003). The aqueductus vestibuli is a small lemoinei and Caenolestes are nearly circular in shape horizontal fissure, located on the medial side and at the (Fig. 6a, c, f). In P. lemoinei, the ratio between length and level of the subarcuate fossa. This opening would transmit the width of the semicircular canals is nearly unity, conse- the endolymphatic duct and accompanying vein from the quently the canals are nearly circular. The length is defined vestibular cavity (MacIntyre 1972; Wible 1990, 2003). The as the distance between the mid-point of the arch of the aqueductus cochleae (=cochlear canaliculus) is a small canal that is the farthest away from the vestibulum to the fissure opening medial to the internal acoustic meatus. The vestibulum, while the width is the greatest dimension per- aqueductus cochleae would transmit the perilymphatic duct pendicular to the length. In P. lemoinei the ASC length/ and accompanying vein from the inner ear cavity to the width is 0.97—estimation after restoration—, the LSC endocranium (MacIntyre 1972; Wible 1990, 2003). length/width is 0.97, and the PSC length/width is 0.89. In The cerebellar view of the petrosal (Figs. 4b, 5b) shows Caenolestes, the ASC length/width is 0.96, the LSC length/ two well-defined grooves that would correspond to the width is 0.91, and the PSC length/width is 0.93. Skeleton of the marsupial Palaeothentes lemoinei A. M. Forasiepi et al. b Fig. 6 Palaeothentes lemoinei (MPM-PV 3566). Model of the At the junction between the semicircular canals and the osseous labyrinth based on 3D reconstructions from micro-CT data ventricule are the three ampullae (Fig. 6c). The anterior in lateral (a), anterior (b), dorsal (c), ventral (d), medial (e), and posterior (f) views. aa anterior ampulla, ac aqueductus cochleae, asc ampulla is on the anteroventral arm of the ASC and dor- anterior semicircular canal, asc anterior semicircular canal, av solateral to the vestibulum, the lateral ampulla is on the aqueductus vestibuli, c cochlea, cc crus commune, fc fenestra anterior arm of the LSC and dorsolateral to the vestibulum, cochleae (=round window), fv fenestra vestibuli (=oval window), la and the posterior ampulla is on the ventral arm of the PSC lateral ampulla, lsc lateral semicircular canal, pa posterior ampulla, psc posterior semicircular canal, v vestibule and ventromedial to the vestibulum. The crus commune is shorter than the length of the ASC (Fig. 6a) in P. lemoinei and Caenolestes. The posterior arm of the LSC and the The ASC slightly projects dorsally from the dorsal-most ventral arm of the PSC join in a short canal and form a point of the PSC (Figs. 6b, 7b) in both paucituberculatans ‘‘second crus commune’’ (Schmelzle et al. 2007; Horovitz studied. The ratio between the extension of the dorsal pro- et al. 2008, 2009)inP. lemoinei (Fig. 6a) and in Caeno- jection of the ASC (i.e., distance between the dorsal-most lestes (Fig. 7c). The endocranial aperture of the aqueductus point of the ASC to the dorsal-most point of the PSC)/height vestibuli is on the crus commune (Fig. 6e, f). of PSC (measured in straight line from the LSC to the Dentary. The left dentary is almost complete except in dorsal-most point of the PSC) is 0.20 in both taxa. The lacking the condylar process (Fig. 8a–c), whereas the right lateral extension of the LSC in P. lemoinei and Caenolestes dentary is represented by only the posterior portion is the same as the lateral extension of the PSC (Figs. 6c, 7c). (Fig. 8d–g). The horizontal ramus is deep, especially at the

Fig. 7 Model of the osseous labyrinth based on 3D reconstructions from micro-CT data of Caenolestes sp. (a–f) and Dromiciops gliroides (g–l) in lateral (a, g), anterior (b, h), dorsal (c, i), ventral (d, j), medial (e, j), and posterior (f, l) views Skeleton of the marsupial Palaeothentes lemoinei

Fig. 8 Palaeothentes lemoinei (MPM-PV 3566). Left dentary in lateral (a), lingual (b), and occlusal (c) views. Scale bar 10 mm. Fragment of right dentary in lateral (d), lingual (e), occlusal (f), and ventral (g) views. Scale bars 5mm level of the molars (Table 1). An alveolus for the hyper- while the angle is about 90° in Lestoros (Martin 2013). The trophied incisor occupies the entire anterior face of the masseteric fossa is broad and deep. There is no masseteric dentary. The dorsal and ventral borders of the horizontal foramen. Among paucituberculatans, this opening was ramus are dorsally curved. There are two similar-sized described for living and extinct taxa: Caenolestes follow- mental foramina (Fig. 8a), as occurs generally in paucitu- ing Osgood (1921) and Abderites following Abello and berculatans (Marshall 1980): one is located at the level of Rubilar-Rogers (2012). the p2 and the other at the level of the trigonid of m1. The In medial view (Fig. 8b), the symphysis extends poste- retromolar space, as seen in lateral view, is very short (i.e., riorly to the level of the anterior border of p3. The man- the last molar is located very close to the anterior coronoid dibular foramen opens posterior to the mid-point of the border). The lower teeth form a medially concave arch in coronoid process. occlusal view (Fig. 8c). The vertical process of the dentary The articular process is preserved on the right dentary. It is more than double the height of the horizontal process. is high and its position suggests that the condyle was The coronoid process is laminar and medially inflected. located well above the alveolar level (Fig. 8d, e). The The anterior coronoid border rises at about 110° respect to angular process is shelf-like (sensu Sa´nchez-Villagra and the alveolar plane (Fig. 8a, e). Among living species, an Smith 1997), and medially inflected, forming a small obtuse angle is found in Caenolestes and Rhyncholestes, platform (Fig. 8f, g). A. M. Forasiepi et al.

Dentition closely related taxa (Marshall 1980; Abello 2007; Goin et al. 2009; Forasiepi et al. 2013). The four following teeth The dentition in MPM-PV 3566 is in a very advanced stage are small and simple in morphology. The teeth decrease in of wear. Several structures are completely worn and the size from the first to the fourth element. In lateral view, morphology is interpreted according to the general shape and these four teeth have collinear alveoli, with no lingual the preserved bases of cusps. Detailed descriptions on the displacement at the second locus. The p3 is two-rooted, morphology of the dentition of P. lemoinei are in Marshall conspicuously larger than the preceding tooth and smaller (1980), Bown and Fleagle (1993), and Abello (2007). than the m1. The molars decrease in size from m1 to m4, although the gradient is less steep than in P. aratae. In m1, Upper dentition. The upper dental formula is: I3 C1 P3 M4 the angle of the trigonid is obtuse (the paraconid has an (Fig. 3a). There is no diastema between the incisors. The anterior position), while in posterior molars the trigonid has first (mesial) incisor (homologous to the I1 of other me- an acute angle, that is, the paracristid is oriented more tatherians; Abello 2013) is the largest among the elements, mesiodistally in m1 than in m4. The m1 trigonid and slightly recumbent, with its tip extending ventrally about talonid are of similar length; in contrast, in P. aratae the three times further than the posterior incisors. The I1 is m1 trigonid is proportionally longer than the talonid. heavily worn especially on its distal side. The second (I2) and third incisors (I3) are much smaller and placed distal and labial to I1. Both I1–I2 are similar in width, contrary to Postcranium the condition in Acdestis maddeni in which the I2 is more laterally compressed (Goin et al. 2003). There is a short The postcranium is represented by several elements of the diastema between the last incisor and the canine, as in A. axial and appendicular skeleton. The axial skeleton is maddeni (Goin et al. 2003). represented by 16 vertebrae belonging to the cervical, The canine is small, although larger than the following dorsal, sacral, and caudal regions (Fig. 9), and by frag- premolar, and labiolingually compressed (Fig. 3b). A small mentary ribs. The appendicular skeleton is represented by a distema separates it from the P1. left humerus and ulna, both radii, the right pelvis, right The P1–P3 have two roots. A small diastema separates femur, right astragalus, metapodials, and phalanxes. We P1 from P2. P1 is the smallest premolar. P2 has a central concentrate here in the anatomy of the appendicular bones, high cusp and a much smaller posterior one. P3 is the as they provide useful characters for comparisons with largest premolar. Labially the P3 develops a high, sub- other metatherians. Further descriptions on the morphology horizontal and trenchant edge. of the postcranium of P. lemoinei are to be found in Abello Molars decrease rapidly in size from M1 to M4. Because and Candela (2010) and Abello et al. (2012). of wear, cusp features are not visible. The crowns are la- Humerus. The left humerus is complete except for some biolingually wide compared to mesiodistal length. The M1 damage to the proximal part of the shaft (Fig. 10a, b). The has a subquadrangular shape owing to a large metaconule. head is displaced ninety degrees from its anatomical The posterior molars are subtriangular. The protocones position. No parts of the shaft are missing, although it is protrude lingually, especially in M1 where there is also a anteroposteriorly compressed and a fracture distorts it from perpendicular crest between the anterolingual and pos- its original shape (the shaft in Palaeothentes minutus terolingual faces of the protocone. Considering the labial described by Abello and Candela 2010, Fig. 1, is more contour of the molars, two main stylar cusps were present: slender than in MPM-PV 3566). StB and StC ? D (according to the homologies established The humerus is 76 % the length of the femur (Table 2). for other paucituberculatans; Abello 2007, 2013; Abello The humeral head is ovoid, dorsoventrally elongate and and Rubilar-Rogers 2012). mediolaterally compressed with a length/width ratio of Lower dentition. There are six antemolar teeth in the den- 1.36. The greater tuberosity is low relative to the projection tary (Fig. 8a, c). The homologies of these teeth are difficult of the humeral head, similar to Lestoros. A crest for the m. to establish. Ontogenetic evidence also makes the identi- teres major is absent. The deltopectoral crest is broken and fication of the antemolar teeth tentative (Luckett and Hong crushed proximally (Fig. 10a). Distally, the crest is raised 2000). It has been proposed that the teeth lost in the Pal- and somewhat flattened suggesting that it formed a shelf aeothentidae are the combination of i4, i5, c, p1 or p2 (following Horovitz and Sa´nchez-Villagra 2003). How- (Abello 2007, 2013). Here we follow previous authors in ever, the preserved parts are very unlike the condition in interpreting the hypertrophied lower incisor and its Lestoros in which the deltopectoral shelf is broad and flat. immediately distal tooth as i2 and i3, respectively (Hersh- Our reconstruction of the length of the deltopectoral crest is kovitz 1995; Abello 2007). In MPM-PV 3566, the i2 is about 15.9 mm, for a ratio of 42 % with the total humeral large and procumbent, as in other paucituberculatans and length. This crest does not extend as far distally on the shaft Skeleton of the marsupial Palaeothentes lemoinei

Fig. 9 Palaeothentes lemoinei (MPM-PV 3566). Two cervical vertebrae (a–d), the second sacral vertebra (e, f), one distal caudal vertebra (g, h) in dorsal and ventral views. Scale bar 10 mm as in Lestoros and Rhyncholestes. The ectepicondylar crest is coronoid process. Together, the two processes define a narrow (i.e., not salient) and long, representing 52 % of total deep trochlear notch. The trochlear notch index (following the length of the bone (Fig. 10b). This differs from the short Szalay and Sargis 2001) is estimated to be 42. This value is crest of Lestoros (ratio between ectepicondylar crest 4.8 mm/ similar to the value of 46 reported for P. minutus (Abello total humeral length 16.25 mm = 29 %) and the narrower and Candela 2010) and the 44 reported for Rhyncholestes crest of Rhyncholestes and Caenolestes (Osgood 1921;Szalay (Szalay and Sargis 2001). The medial portion of the ulnar and Sargis 2001). There is a large entepicondylar foramen. proximal trochlear crest is widened and strongly sigmoid in The supracondyloid crest partially covers the foramen, and the shape and the ulnar cranial olecranon ridge is displaced opening is not fully visible in anterior view, a difference from medially in P. lemoinei,asinCaenolestes and Rhyncho- living caenolestids in which the foramen opens anteriorly lestes (Szalay and Sargis 2001). The radial notch is offset (Abello and Candela 2010). laterally. The shaft of the ulna is mediolaterally com- The medial epicondyle is even more reduced than in pressed and curves anteriorly. Shallow grooves are devel- Caenolestes and Rhyncholestes (Osgood 1921; Szalay and oped on the lateral and medial sides of the shaft. Sargis 2001). The capitulum is ovoid and is less distally pro- Radius. Both the right and left radius have been pre- truding compared to the trochlea. The coronoid fossa and radial served, with the left element is in better condition fossa form a continuous depression. The trochlea is ovoid in (Fig. 10e, f). The radius is shorter than the ulna (about the distal view. As in Lestoros, the distal articular surface of P. 79 % of the total length of the ulna, Table 2) and antero- lemoinei is extensive and bulges to form a ‘pseudocapitulum’ posteriorly compressed. The radial head is suboval in extending far medially to engulf most of the medial epicon- proximal view. The bicipital tuberosity is robust, oval, dyle. Sharp edges define the articular area in anterior and strongly posteriorly protruded and placed close to the radial posterior view. In posterior view, the olecranon fossa is shifted head (Fig. 10f), as described for P. minutus. The radial laterally. It is deeper compared to Lestoros.InP. minutus the shaft in P. lemoinei (Fig. 10e, f) is slightly curved, in olecranon fossa is perforated (Abello and Candela 2010). contrast to the almost straight and slender shaft of P. minutus (Abello and Candela 2010). The styloid process is Ulna. The left ulna is well preserved except for lacking the distal triangular and distally projected. In ventral view the distal part of the shaft and distal epiphysis (Fig. 10c, d). The olecranon epiphysis is shallowly concave and bears an oval and process is relatively short and would comprise between 11 and oblique facet for articulation with the scaphoid bone, which 12 % the length of the bone (total length of the ulna estimated extends from the distal surface of the epiphysis to the lat- with the length of the radius; Table 2). This proportion of the eral surface of the styloid process. The relation between the olecranon is smaller than in Caenolestes (from facets is gently curved (i.e., there is no trochlea). Osgood’s—1921—figures, the olecranon process com- prises about 16 % of the total length of the ulna). The Pelvis. The right pelvis is partially preserved, missing the anconeal process is stout and sharp, as is the lateral anterior part of the illium and the pelvic symphysis A. M. Forasiepi et al.

Fig. 10 Palaeothentes lemoinei (MPM-PV 3566). Left humerus in (f) views. Right pelvis in lateral (g) and medial (h) views. Right femur anterior (a) and posterior (b) views. Incomplete left ulna in medial in anterior (i) and posterior (j) views. Proximal portion of fibula in (c) and lateral (d) views. Left radius in anterior (e) and posterior medial view (k). Scale bar 10 mm

(Fig. 10g, h). The iliac wing is well developed and flat- forms the antero-dorsal border of the gluteal fossa. Because tened anteriorly. The gluteal fossa is larger than the iliac of the preservation, we cannot determine if the greater fossa. The acetabular crest runs from the tubercle of the sciatic notch was deep (if the iliac crest abruptly joins the rectus femoris towards the iliac crest. The acetabular crest caudal dorso-border of the illium) or shallow as in is robust and taller on the anterior part of the wing and Caenolestes (Osgood 1921). The ischial tubercle is distinct separates the gluteal and iliac fossa. The tubercle of the and the lesser sciatic notch is slightly deeper than in rectus femoris is elongated and salient. The iliac crest Caenolestes (Osgood 1921). The iliopubic eminence is Skeleton of the marsupial Palaeothentes lemoinei

Table 2 Measurements of the postcranial elements (in mm) Femur. The femoral head (Fig. 10i, j) is round in dorsal Humerus view, the greater trochanter projects proximally beyond the level of the femoral head, similar to living caenolestids Maximum length (restored) 36a (Osgood 1921; Szalay and Sargis 2001; Abello and Candela Humeral head dorsoventral length 7.67 2010). The trochanteric fossa is straight and long, as in other Humeral head mediolateral breadth 5.63 species of Palaeothentes (Abello and Candela 2010). The Breadth of the proximal epiphysis 9.6a lesser trochanter is flat and triangular in shape similar to Medial epicondyle length 4.65 Caenolestes and Rhyncholestes (Osgood 1921; Szalay and Breadth of distal epiphysis (excluding medial 8.9 epicondyle) Sargis 2001). There is a third trochanter on the lateral side Entepicondylar crest 14.5 9 27.85 of the femur, as in living and paucituberculatans Ulna (Szalay and Sargis 2001; Abello and Candela 2010) and a marsupials from the of Itaboraı´ (Szalay and Maximum length (restored based on the radius) 41.4–45.8 Sargis 2001). The shaft is slightly dorsomedially com- Olecranon process length 5.01 pressed resulting from preservation, although it is clearly Olecranon process breadth 4.5 seen that the lateral and medial borders of the femur are Radius almost parallel. On the posterior aspect, the medial condyle Maximun length 36.35 is slightly wider than the lateral one (FCWI, 103; Table 2). Breadth of proximal epiphysis 3.86 Wide medial condyles are present in Rhyncholestes (FCWI, Breadth of distal epiphysis 5 95; from Szalay and Sargis 2001) and Caenolestes (FCWI, Femur 84; from Osgood 1921, Fig. 12). The intercondylar fossa is Maximum length 49 narrow and deep, and there is a shallow intercondylar notch. Breadth of the proximal epiphysis 10.77 Breadth of the distal epiphysis 9.27 Fibula. Only the proximal part of the fibula is preserved FCWI (femoral condyle width index, medial condyle 103 (Fig. 10k). The shaft is slender and according to the part width/lateral condyle width 9 100 preserved, it was slightly curved. Proximally it is some- Fibula what expanded anteroposteriorly, although not as much as Breadth of the distal epiphysis 5.2 in didelphids (Szalay and Sargis 2001). Astragalus Astragalus. Only the right astragalus has been preserved Maximum anteroposterior length 6.65 (Fig. 11). In dorsal view (Fig. 11a), the dominant facets are Anteroposterior length of ectal facet 3 the astragalofibular facet (AFi) and lateral astragalotibial Medial breadth of ectal facet 4.9 facet (ATil). Both facets form a continuous surface with a Breadth of neck 2.5 narrow sulcus between forming a barely defined trochlea. Neck length 3.65 The angle between the AFi and the ATil is approximately Autopodium 180°,asinCaenolestes. The ATil is at about 90° from the Maximum length metacarpal a 9 medial astragalotibial facet (ATim) and there is a promi- a Maximum length metacarpal b (no smaller than) 9.04 nent medial trochlear crest between the two, as in Caeno- Maximun length MCV 7 lestes. There is also a lateral trochlear crest on the lateral Maximun length metatarsal d 20 edge of the AFi. Whereas in Caenolestes the medial and Maximum length metatarsal e (no smaller than) 20.05a lateral trochlear crests are almost parallel, in P. lemoinei Maximum length phalanx (no smaller than) 7.7a they are at different angles. There is a projection of the a The measurement is approximated ATim towards its medial border, absent in Caenolestes (Szalay 1994), and consequently the ATim is wider in the distal portion than in the proximal part, the opposite being well defined as in Caenolestes and , instead of the case in Caenolestes (Szalay 1994). Similarly, there is a being strongly developed as in macropodids among mar- distolateral expansion of the AFi, as is common among supials (Horovitz and Sa´nchez-Villagra 2003). The cranial marsupials, including Caenolestes (Szalay, 1994), but portion of the acetabular area is somewhat distorted. This is absent in many eutherians (e.g., Salton and Szalay 2004, a deep area with well-defined borders. Posteroventrally, the Fig. 3). The astragalar neck is clearly defined; it is as wide lunate surface is interrupted by a deep acetabular notch. or slightly wider than the head, as in other metatherians The acetabular fossa was apparently round. The obturator (Horovitz 2000). A well-defined astragalotibial pit is foramen is incomplete but considering the borders pre- located at the dorsal base of the neck. The astragonavicular served the opening was oval with a ventral projection as in facet (AN) extends on the ventromedial area of the head. Caenolestes (Osgood 1921). In distal view, the AN is wider transversely than A. M. Forasiepi et al.

Fig. 11 Palaeothentes lemoinei (MPM-PV 3566). Right astragalus in dorsal (a) and plantar (b) views dorsoventrally, as in Caenolestes. The AN is confluent with the sustentacular facet as in living caenolestids (Abello and Candela 2010). In plantar view (Fig. 11b), the sustentacular facet is broad and slightly convex; it does not reach the medial edge of the astragalar neck. The AN is positioned anterior relative to the facets for the tibia and not medial to them as in at least some macropodoids among marsupials (Horovitz and Sa´nchez-Villagra 2003). The astragalar canal, which is present in Yalkaparidon and some das- Fig. 12 Palaeothentes lemoinei (MPM-PV 3566). Metacarpals (a–c), yurids among marsupials (Szalay 1994; Horovitz and metatarsals (d–f), and phalanx (f). Scale bar for a, b, c, f = 5 mm. Sa´nchez-Villagra 2003, Beck et al. 2013), is absent in P. Scale bar for d, e = 10 mm lemoinei. The longer dimension of the astragalocalcaneal facet (CaA) is orientated posteromedial to anterolaterally, Discussion as in Caenolestes and most marsupials. This facet is concave and extends to the posterior edge of the astra- Skull and dentition galus as in Caenolestes. The astragalar medial plantar tuberosity (ampt) is large although not visible in dorsal The dental morphology of palaeothentids is more derived view. than that of caenolestids (Goin et al. 2003), but the skull Metapodials and phalanxes. The elements of the autopo- has more plesiomorphic traits, as shown by the study of dium are disarticulated. The metacarpals (Fig. 12a–c) are MPM-PV 3566. The skull of Palaeothentes lemoinei is shorter and more robust than the metatarsals. A short ele- larger than extant caenolestids, with a shorter and broader ment with an oblique proximal articular facet and an snout, smaller palatal vacuities, proportionally narrower asymmetrical trochlea (Fig. 12c) is interpreted as the fifth interorbital constriction, and a less globular and more tri- left metacarpal, based on comparisons with didelphids (see angular-shaped cranial vault in dorsal view. These features also Szalay and Sargis 2001). The two remaining are are shared with other Miocene paucituberculatans, such as similar sized (Table 2). The symmetrical trochlea is well- the palaeothentids Palaeothentes minutus, Acdestis oweni, preserved in one of them (Fig. 12a) and suggests that they and A. maddeni (Sinclair 1906; Goin et al. 2003). In con- could belong to mid-fingers (metacarpal second, third or trast, the dentition demonstrates unique features such as the forth). The metatarsals are very slender, long and with reduction in number of the incisors, a p3/m1 shearing straight shaft (Fig. 12d, e). The proximal epiphysis is complex (although not to the extreme development of a dorso-plantarly deep and narrow latero-medially. The plagiaulacoid m1 as in abderitids), and the molars with trochlea is symmetrical with a well pronounced sagittal steeper size gradient from front to back (Marshall 1980; crest. One fragmentary phalanx (Fig. 12f) is interpreted Bown and Fleagle 1993; Abello 2007). from the anterior limb because the size and robustness is The upper antemolar teeth are partially known in other similar to the metacarpals. The shaft is broader proximally palaeothentids (Abello 2013). MPM-PV 3566 clearly has than distally. seven upper antemolars as was inferred based on previous Skeleton of the marsupial Palaeothentes lemoinei specimens (Acdestis maddeni following Goin et al. 2003, Diprotodon, Thylacoleo, and living marsupials including and some specimens referred to Palaeothentes minutus, didelphids, dasyurids, and paramelids (Sa´nchez-Villagra following Abello 2007) and whose homologies are con- and Schmelzle 2007; Schmelzle et al. 2007; Horovitz et al. sidered to be I1–I3 C P1–P3 (Abello 2013). MPM-PV 3566 2008, 2009; Alloing-Se´guier et al. 2013) and is reportedly has six lower antemolar teeth as in other palaeothentids plesiomorphic for Mammaliaformes (Ruf et al. 2013). Its (Abello 2013), the homologies of which are not certain for finding in P. lemoinei further suggests a broader distribu- all of them (for a discussion about this topic, see Abello tion of this character among metatherians. 2013). P. lemoinei is a medium sized taxon (about 350 g; The limited but valuable knowledge provided by the few Abello et al. 2012), similar in body mass to Pseudocheirus and incomplete known skulls of fossil paucituberculatans canescens among extant marsupials (Smith et al. 2003). It serves for comparisons with the new specimen of P. lemoinei has been demonstrated that the shape of the osseous (MPM-PV 3566). P. lemoinei differs from the Acdestis labyrinth has a strong allometric relationship (Alloing- maddeni and A. oweni by a narrower interorbital constric- Se´guier et al. 2013) and comparisons with the available tion. For Acdestis maddeni, Goin et al. (2003) estimated an data suggest that P. lemoinei is no exception. The laby- interorbital constriction width of 8.7 mm, ca. 1 mm wider rinths in larger marsupials have (1) the ASC and PSC than in MPM-PV 3566 although that skull of Acdestis proportionally larger and the LSC proportionally less maddeni (condylo-basal length 53.8 mm) is 10 mm smaller developed, (2) the cochlea relatively smaller and laterally (85 % of MPM-PV 3566’s size). Nasals are narrower in P. oriented, and (3) a longer crus commune (Alloing-Se´guier lemoinei than in Acdestis oweni and crests on the dorsal et al. 2013). In P. lemoinei, in accordance with its body surface of the cranial vault are intermediate between A. size, no allometrically unexpected differences have been maddeni with low crests and A. oweni with taller crests. detected in the size of the semicircular canals; the spiral of Until now, only Acdestis maddeni from the Middle the cochlea represents a large portion of the osseous Miocene (Laventan) of Bolivia (Goin et al. 2003) has labyrinth, and ASC and PSC bifurcate distantly from their provided information about the ear region of fossil pauci- most extent dorsal border, resulting in a relative short crus tuberculatans. P. lemoinei provides further details of this commune (in clear contrast, the ASC and PSC bifurcate at area, in particular the petrosal and osseous inner ear anat- the level of the dorsal border of the semicircular canals in omy. Uniquely to date for a fossil South American mar- Diprotodon, resulting in a long crus commune; Alloing- supial, MPM-PV 3566 has been subject to a micro-CT Se´guier et al. 2013). scan. The shape of the semicircular canals reflects the mem- In P. lemoinei, the cochlea has 1.9 turns similar to branous ducts within. The semicircular canals of the ves- Caenolestes with 2 turns. This number is close to, but tibular system are involved in the perception of changes in slightly outside the range commonly found in living mar- the rotational acceleration of the head (Malinzak et al. supials in which the cochlea has between 2.4 and 3 turns 2012). Only two studies have examined the correspondence (Sa´nchez-Villagra and Schmelzle 2007, e.g., Dromiciops between the size and shape of the semicircular canals and with 2.5 turns: Fig. 7h). In contrast, stem marsupials have a locomotion specifically in marsupials, and in particular in less coiled cochlea, such as Herpetotherium with 1.6 turns diprotodontians (Schmelzle et al. 2007; Alloing-Se´guier (Horovitz et al. 2008), a metatherian from et al. 2013). The postcranial anatomy of P. lemoinei sug- Montana with 1.5 turns (Meng and Fox 1995), and gests that this species was an agile terrestrial marsupial exceptionally some australidelphians such as Vombatus (Abello and Candela 2010; Abello et al. 2012; see also ursinus with 1.4 turns (Sa´nchez-Villagra and Schmelzle below), and, therefore, the morphology of the semicircular 2007) and Notoryctes with 1.6 turns (Ladeve`ze et al. 2008). canals may correlate with a precise coordination. The osseous labyrinth of P. lemoinei exhibits a ‘‘second In P. lemoinei as in Caenolestes, the ASC projects crus commune’’. Usually, the vestibulum is pierced by five slightly dorsally from the dorsal-most point of the PSC openings that lead to (1) the crus commune, (2) the anterior (Fig. 6a) and the ratio between the extension of the dorsal arm of the ASC, (3) the anterior arm of the LSC, (4) the projection of the ASC/height of PSC is 0.20. This esti- posterior arm of the LSC, and (5) the inferior arm of the mation is in the range of quadruped species (see Schmelzle PSC, as occurs in Dromiciops among the taxa studied here et al. 2007 for a discussion of this character and compar- (Fig. 7a, g). However, in some marsupials, as P. lemoinei, isons between marsupials). In diprotodontians bipedal and Caenolestes there are four openings by the common species with erected posture (i.e., Bettongia, Dorcopsis, entrance of the posterior arm of the LSC and the inferior and Macropus) this ratio is larger than 0.42 (Schmelzle arm of the PSC through a ‘‘second crus commune’’ (Sch- et al. 2007). melzle et al. 2007). A ‘‘second crus commune’’ was In P. lemoinei, the extension of the LSC is the same as described for Herpetotherium, , the lateral extension of the PSC (Fig. 6c), as it is in A. M. Forasiepi et al.

Caenolestes (Fig. 7c). This condition has been found in of the femoral head, and (3) a reduced lesser trochanter, species with precise coordination, such as the arboreal taxa and (4) a third trochanter, (5) lateral condyle slightly nar- (e.g., Dromiciops; Fig. 7i), or in taxa that use a smaller and rower than medial one, (6) astragalus with a strong angle more complex substrate (i.e., smaller and more exact steps; between the ATil and ATim facets, and (6) a slightly Schmelzle et al. 2007). This character may be correlated to grooved trochlea. The last feature is unique among the locomotion; however, it has also been found to vary in- known fossil metatherians from South America. No traspecifically and it is strongly influenced by body size grooved trochlea has been found in the and phylogeny (Schmelzle et al. 2007; Alloing-Se´guier (Argot 2004; Forasiepi 2009) a group represented by ter- et al. 2013). We report a similar length of the LSC and PSC restrial species, even though some species achieved a in both paucituberculatans, closer phylogenetically and of certain degree of cursoriality (Argot 2004; Ercoli and similar locomotion. Prevosti 2012). The presence of a trochlear groove and lateral and medial crests surrounding the ATil and AFi Postcranium indicates some degree of restriction of mediolateral mobility of the lower ankle joint and facilitation of stability Only two partial skeletons of fossil pauciturberculatans are in flexion and extension (Szalay 1994, and references known to date, those of P. minutus (MACN 5619–5639) therein). As reviewed and studied in a wide range of and P. lemoinei (MPM-PV 3494) (Abello and Candela mammals by Szalay and other authors (e.g., Szalay 1994; 2010; Abello et al. 2012). The new specimen (MPM-PV Nakatsukasa et al. 1997; Szalay and Sargis 2001), the 3566) has provided information about the anatomy of the shape and configuration of the astragalus reflects not only radius, femur, and metapodials of P. lemoinei and addi- phylogenetic history but also the direction and distribution tional information about the pelvic girdle. of incurred loads from the crus. The paleobiology of Palaeothentes, including the loco- motion, was analysed by Abello and Candela (2010) and Abello et al. (2012) on the basis of postcranial remains of Conclusion P. minutus and P. lemoinei. These studies suggested that Palaeothentes would have been an agile cursorial dweller Compared to that of living caenolestids, the skull of with leaping ability, similar to Caenolestes, Lestoros, and Palaeothentes lemoinei has more plesiomorphic traits in the didelphid Metachirus (Abello and Candela 2010; the face, palate, and cranial vault than living paucituber- Abello et al. 2012). The study of MPM-PV 3566 supports culatans; whereas the dental morphology is more derived. this conclusion. Considering the characters previously The analysis of the osseous inner ear revealed a cochlea analysed that are informative for paleobiological recon- with 1.9 turns, the presence of a second ‘‘crus commune’’, structions (Szalay and Sargis 2001; Abello and Candela an ASC projecting slightly dorsally from the dorsal-most 2010; Abello et al. 2012), the new specimen of P. lemonei point of the PSC, and an LSC and PSC projecting laterally has the following in the forelimb: (1) humerus with a rel- up to the same level. atively short deltopectoral crest, (2) short ectepicondylar The specimen provides new information about the crest, (3) poorly protruding medial epicondyle, (4) high and anatomy of the radius, pelvic girdle, femur, and metapo- deep humeral trochlea, and its correspondence in the ulna dials. Previous studies have demonstrated that P. lemoinei with a deep and close trochlear notch, with protruding was an agile cursorial dweller and we supported this borders, (5) the ulna with short olecranon process, (6) inference with the new data. suboval radial head, and (7) large and protruding bicipital tuberosity. Those features are present in living terrestrial Acknowledgments We thank Scott Moore-Fay (NHM, London) for marsupials (e.g., caenolestids as well as Metachirus, the preparation of the isolated petrosal and the dentary of MPM-PV 3566, and Phil Crabb (NHM, London) for photography. Dromiciops gliro- latter an agile, cursorial-to-saltatorial ), supporting ides was scanned by A. Mazurier (Univ. Poitiers, Society E.R.M. the paleocological interpretation of P. lemoinei as a mainly Poitiers). Dr. Robin Beck provided useful comments that helped to terrestrial (Abello and Candela 2010). Differing improve the original manuscript. Field work to Santa Cruz Formation from the described morphology of P. minutus (Abello and was supported by a National Geographic Society grant to Sergio Vizcaı´no and RFK, National Science Foundation grant BNS-0824546 Candela 2010; Abello et al. 2012), MPM-PV 3566 has a TO RFK and PICT 0143 (to Sergio Vizcaı´no). curved ulnar and radial shaft and a wider radial shaft. This could represent intraspecific variation, although the possi- bility of taphonomic distortion affecting the real shape of References the bone cannot be ruled out. In the hindlimb, (1) the pelvis has a deep acetabulum with protruding borders, (2) the Abello, M. A. (2007). Sistema´tica y bioestratigrafı´a de los Paucitu- femur has a greater trochanter projecting beyond the level berculata (Mammalia, Marsupialia) del Cenozoico de Ame´rica Skeleton of the marsupial Palaeothentes lemoinei

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